Woodcreeper species continue to exchange DNA until 2.5 million years after divergence

Recent study estimates the time window for introgression in birds.

One of my favorite avian hybrids is the Swoose, a cross between a Greylag Goose (Anser anser) and a Mute Swan (Cygnus olor). This particular hybrid is probably sterile, because its parental species diverged more than 20 million years ago. It has been estimated that bird species can still produce viable offspring after, on average, 21 million years of independent evolution. This is considerably longer compared to mammals, where it takes about 4 million years for hybrid inviability to develop. The time window for hybridization has thus been established for birds and mammals, but what about introgression? How long can hybridization result in the exchange of genetic material between species? A recent study in the journal Evolution tackled this question using the neotropical genus Dendrocincla.

Dendrocincla_fuliginosa

 

ABBA-BABA

Paola Pulido‐Santacruz and her colleagues collected genomic data for 87 specimens, representing all six recognized species in this genus. First, they reconstructed the phylogenetic relationships between these taxa. The resulting evolutionary tree served as the backbone for a series of ABBA-BABA-tests to infer introgression. For readers unfamilar with this approach, I copied the explanation from a previous blog post (D-statistics for Dummies).

The rationale behind this test is quite straightforward: it considers ancestral (‘A’) and derived (‘B’) alleles across the genomes of four taxa. Under the scenario without introgression, two particular allelic patterns ‘ABBA’ and ‘BABA’ should occur equally frequent. An excess of either ABBA or BABA, resulting in a D-statistic that is significantly different from zero, is indicative of gene flow between two taxa. A positive D-statistic (i.e. an excess of ABBA) points to introgression between P2 and P3, whereas a negative D-statistic (i.e. an excess of BABA) points to introgression between P1 and P3.

The figure below illustrates this procedure for several Dendrocincla subspecies. In this example, there is an excess of ABBA-patterns, suggesting introgression between the subspecies neglecta and ridgwayi (belonging to the Plain-brown Woodcreeper, D. fuliginosa).

ABBABA_dendro

The ABBA-BABA-test was used to infer introgression between different Dendrocincla (sub)species. Here, an excess of ABBA-patterns points to introgression between the subspecies neglecta and ridgwayi (indicated with black arrows). From: Pulido-Santacruz et al. (2020) Evolution.

 

Time Window

These analyses uncovered five introgression events, which is probably an underestimate because the ABBA-BABA-test only captures introgression between nonsister taxa. Nonetheless, the researchers were able to date these introgression events, which ranged from “a few hunderd thousand to about 2.5 million years following divergence”. These results suggest that the timeframe for introgression is much narrower than the timeframe for hybridization. In Dendrocincla woodcreepers, the species boundaries seem to become impermeable after about 2.5 million years of separate evolution. Whether this time window is the same for other bird species remains to be tested.

dendro_tree

The phylogenetic tree of the genus Dendrocincla with different introgression events indicated with colored arrows. From: Pulido-Santacruz et al. (2020) Evolution.

 

Genetic Snowballs

Another interesting observation in this study concerns the amount of genetic material than is exchanged between species. I explained the relevance of this pattern in a news article (a so-called digest) that accompanies the original study: “These proportions turned out to decline exponentially with the age of the hybridizing taxa. Interestingly, this pattern resembles the accumulation of genetic incompatibilities during the build-up of postzygotic isolation. These genetic incompatibilities do not increase linearly but instead seem to snowball because each new mutation is increasingly likely to be incompatible with a previous mutation.” However, this pattern is based on a few datapoints and will need to be confirmed with more data and other species.

dendro_curve

The relationship between the proportion of DNA exchanged (fhom) and the age at hybridization follows a snowball pattern, reminiscent of the accumulation of genetic incompatibilities. From: Pulido-Santacruz et al. (2020) Evolution.

 

References

Ottenburghs, J. (2020). Digest: Avian genomes are permeable to introgression for a few million years. Evolution.

Pulido‐Santacruz, P., Aleixo, A., & Weir, J. T. (2020). Genomic data reveal a protracted window of introgression during the diversification of a Neotropical woodcreeper radiation. Evolution.

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